The bacteriophage T4 has served as an in vitro model for the study of DNA replication for several decades, yet less is known about this process during infection. Our previous work has shown that viral DNA synthesis is initiated from at least five origins of replication distributed across the 172 kb chromosome, but continued synthesis is dependent on recombination. Helicases, proteins that promote DNA strand separation, are required in all organisms both for replication and for recombination. In T4, two proteins are predicted to facilitate loading of the hexameric 41 helicase at the origins of replication, the Dda accessory helicase and the 59 loading protein. Using a real time, genome-wide assay to monitor replication during infections, we have shown that dda mutant viruses no longer preferentially initiate synthesis near the origins, implying that the Dda accessory helicase has a fundamental role in origin selection and activation. In contrast, at least two T4 replication origins function efficiently without the 59 loading protein, indicating that other factors load the 41 helicase at these loci. Hence, normal T4 replication includes two mechanistically distinct classes of origins, one requiring the 59 helicase loader, and a second that does not. Since both mechanisms require an additional factor, repEB, for sustained activation, normal T4 origin function appears to include at least three common elements, origin selection and initial activation, replisome loading, and persistence.